Succeeding his father in the earldom in 1558, Argyll immediately became the most powerful magnate of the kingdom. A devout protestant, he soon became one of the leaders of the Congregation along with his brother-in-law, Lord James Stewart, illegitimate son of James V of Scotland. Together, the two men negotiated with William Cecil to secure English aid against the regent, Mary of Guise, and were largely responsible for the negotiation of the Treaty of Edinburgh in 1560, which saw the triumph of the Congregation and the withdrawal of French and English troops from Scotland.
With the young queen's return to Scotland in 1561, Argyll and Stewart, now Earl of Moray, retained their leading role in the kingdom, continuing to pursue an anglophilic policy. Their pre-eminence came to an end in 1565, with the queen's marriage to Henry Stuart, Lord Darnley, whose claims to the English throne did not endear him to Elizabeth I of England, leading Argyll and other protestant leaders to rise in revolt. When the English failed to help their Scottish allies, Argyll, who alone of the rebels was able to remain in the Kingdom, due to his inassailable position in the Highlansds, began to become disillusioned with his previous anglophilic policy.
Over the next two years, however, the shifts in Argyll's policies remained subtle, and he remained close to his old friend Moray. Argyll was tied to the assassinations of both David Rizzio in 1566 and of the King himself in 1567, and was horrified by the Queen's marriage to James Hepburn, 4th Earl of Bothwell. He joined with Moray and other protestant leaders in fighting Mary and Bothwell in that year, leading to the capture of the queen at Carberry Hill, but broke with his former allies over the question of deposing the queen.
With Mary's escape from prison in 1568, Argyll became the leader of the Queen's Party, and led Mary's army in the defeat at Langside in that year. He continued to champion the queen's cause following her flight to England, but eventually reconciled with the regent Lennox in 1571, and lent his support to the King's party, as a means of restoring peace and lessening English meddling in Scottish affairs.
Argyll, in his role as Campbell clan chief, was also heavily involved in the politics of Ulster during the 1560s. Although he initially hoped for an alliance with the English to secure his O'Donnell and MacDonald dependents against the encroachment of the O'Neill, English unwillingness to work with him ultimately led him to orchestrate a marriage alliance among the three feuding clans of Ulster, which would ultimately have major effects on Irish history with the eruption of the Hugh O'Neill rebellion in the 1590s.
Argyll died in 1573, childless, and was succeeded by his brother Colin.
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